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Novel Bacterial Vaginosis-Associated Organisms Mediate the Relationship Epidemiology Sex Transm Infect: first published as 10.1136/sextrans-2019-054191 on 6 December 2019. Downloaded from ORIGINAL RESEARCH Novel bacterial vaginosis- associated organisms mediate the relationship between vaginal douching and pelvic inflammatory disease Tamala Gondwe ,1 Roberta Ness,2 Patricia A Totten,3 Sabina Astete,3 Gong Tang,4 Melanie A Gold,5 David Martin,6 Catherine L Haggerty 1,7 ► Additional material is ABSTRACT PID, including infertility, ectopic pregnancy, recur- 2 published online only. To view Objectives We sought to determine whether the rent PID and chronic pelvic pain. please visit the journal online relationship between a history of vaginal douching Ness et al previously identified an associa- (http:// dx. doi. org/ 10. 1136/ 3 sextrans- 2019- 054191). and pelvic inflammatory disease (PID) is mediated by tion between vaginal douching and PID. Among endometrial infection with one or more novel bacterial women in the PID Evaluation and Clinical Health For numbered affiliations see vaginosis (BV)- associated organisms among Atopobium (PEACH) study, those who reported douching more end of article. vaginae, the BV- associated bacterium 1 (BVAB1), neathia than once per month were 60% more likely to have (Leptotrichia) amnionii and Sneathia sanguinegens. histologically confirmed endometritis or upper Correspondence to 3 Dr Catherine L Haggerty, Methods We first conducted log- binomial regression genital tract gonorrheal or chlamydial infection. Department of Epidemiology, analyses to identify risk factors for endometrial infection Another study in a similar cohort, the Gynecologic University of Pittsburgh in 535 adolescent and adult women with clinically Infections Follow- Through (GIFT) study found that Graduate School of Public suspected PID in the PID Evaluation and Clinical Health douching for symptoms or hygiene at least once per Health, Pittsburgh, Pennsylvania, (PEACH) study. We then examined whether endometrial month was associated with bacterial vaginosis (BV), PA 15260, USA; haggerty@ 4 pitt. edu infection by the BV- associated organisms mediated the diagnosed using Nugent’s criteria. BV is a common association between a history of vaginal douching and condition among women, with prevalence estimates Received 3 July 2019 histologically confirmed PID using inverse probability ranging from 5% to 36%,5 and is characterised by Revised 27 October 2019 weighted marginal structural models. Accepted 7 November 2019 a shift from a vaginal flora with predominant lacto- Published Online First Results Vaginal douching was significantly associated bacilli to one with high concentrations of a diverse 6 December 2019 with endometrial infection with one or more of the collection/array of other aerobic and anaerobic targeted BV- associated organisms (relative risk (RR) bacteria. These findings support the notion that 1.21, 95% CI: 1.08 to 1.35). The total effect estimate douching disrupts the normal vaginal flora, which, suggested that vaginal douching increased the risk of in turn, promotes colonisation with BV-associated endometritis by 24% (RR 1.24, 95% CI: 1.03 to 1.49). bacteria. Women with BV also have an increased risk The controlled direct effect of this association was of acquiring sexually transmitted infections (STIs), http://sti.bmj.com/ attenuated with endometrial infection by one or more particularly Neisseria gonorrhoeae and Chlamydia BV- associated organisms (adjusted RR (aRR) 1.00, trachomatis, which if left untreated can ascend to 95% CI: 0.57 to 1.74) and endometrial infection by all the upper genital tract and cause PID.6 Although four BV- associated organisms (aRR 0.95, 95% CI: 0.53 to PID is often associated with N. gonorrhoeae and 1.70) as intermediate variables. C. trachomatis infection, up to 70% of PID cases Conclusions Endometrial infection with one or more of are of unknown microbial aetiology, and BV has on September 24, 2021 by guest. Protected copyright. the novel BV- associated organisms partially mediated the been directly associated with PID, independent of relationship between vaginal douching and histologically chlamydial and gonococcal infection.7 confirmed endometritis in the PEACH study. Frequent Using traditional bacterial cultivation methods, vaginal douching may confer risk for endometritis the vaginal flora of women with BV is frequently through increasing the risk of endometrial infection defined by overgrowth of Gardnerella vaginalis, by novel- BV- associated organisms. Other potential Ureaplasma species, Mycoplasma hominis, Mobi- pathways should be explored. luncus species, Prevotella species and several other bacteria, including anaerobes.8 The role of recently identified fastidious vaginal microbes in gyneco- INTRODUCTION logical and reproductive morbidity has not been © Author(s) (or their Pelvic inflammatory disease (PID), the infection and widely researched. Fredericks et al conducted a employer(s)) 2020. Re- use broad range PCR sequencing study among women permitted under CC BY-­NC. No inflammation of a woman’s fallopian tubes (salpin- commercial re-use . See rights gitis) and uterine lining (endometritis), is a frequent aged 18–42 years to identify novel bacteria in and permissions. Published and morbid condition among young women. The vaginal fluid obtained from 27 women with BV and by BMJ. estimated prevalence of PID among sexually experi- 46 women without BV.8 They found a strong associ- To cite: Gondwe T, enced women aged 18–44 years is 4.4%, suggesting ation between BV and Atopobium vaginae, Sneathia Ness R, Totten PA, that approximately 2.5 million reproductive- aged (Leptotrichia) sanguinegens, Sneathia (Leptotrichia) et al. Sex Transm Infect women have ever been diagnosed with PID.1 Major amnionii, and three newly recognised bacteria 2020;96:439–444. reproductive and gynecologic sequelae result from designated Bacterial Vaginosis- associated bacteria Gondwe T, et al. Sex Transm Infect 2020;96:439–444. doi:10.1136/sextrans-2019-054191 439 Epidemiology Sex Transm Infect: first published as 10.1136/sextrans-2019-054191 on 6 December 2019. Downloaded from Figure 1 Illustration of the hypothesised associated pathways in the relationship between a history of vaginal douching twice or more in the past month and endometritis in the PEACH study. PEACH, PID Evaluation and Clinical Health; BV, bacterial vaginosis. (BVAB): BVAB1, BVAB2 and BVAB3. Furthermore, these bacteria sexual activity in the past 4 weeks, number of lifetime sexual were highly prevalent among women with BV compared with partners, new sexual partner in the past 4 weeks, history of STIs, women without BV. history of BV, history of PID, recent hormonal contraceptive use, We previously demonstrated that vaginal douching is associ- condom use, oral sex, anal sex, age at sexual debut, history of ated with an increased likelihood of cervical and/or endometrial vaginal douching practices, drug and alcohol use, and tobacco infection with S. sanguinegens and S. amnionii in the PEACH use. Vaginal douching at baseline was assessed through questions study, and that endometrial infection by the microorganisms is of douching frequency in the past 4 weeks, type of products used associated with an increased likelihood for endometritis.9 We and reasons for douching. This analysis, consistent with prior suspected that endometrial infection by BV-associated organisms studies, assessed vaginal douching as frequency two times or is an intermediate between vaginal douching and endometritis more in the past month (Yes or No). (figure 1). Our objective was to assess the mediation effect of At baseline and at 30 days after enrolment in the parent PEACH endometrial infection by BV- associated organisms in the rela- study, cervical swabs and endometrial biopsies were obtained for tionship between a history of vaginal douching and histologically histology, chlamydial PCR (Roche Diagnostics) and gonococcal confirmed endometritis using data collected from the PEACH culture. Endometrial biopsies were obtained using a sterile, single cohort. use, disposable endometrial suction curette after first swabbing the exocervix twice with betadine and the endocervix once with METHODS betadine. Histological examination was performed on hematox- http://sti.bmj.com/ Study population ylin and eosin- stained and methyl green pyronine stained biopsy We conducted this study using baseline data from the PEACH tissue specimens, read separately by two reference pathologists study. Details of subject recruitment and data collection have who reviewed the slide together to reach consensus on disagree- previously been described.10 In brief, the primary aim of the ment. A modification of the criteria proposed by Kiviat et al was PEACH study was to compare the effectiveness of inpatient used to diagnose endometritis, defined by at least five neutrophils versus outpatient treatment for preventing long- term complica- per ×400 in the endometrial surface epithelium in the absence on September 24, 2021 by guest. Protected copyright. tions of mild-to- moderate PID. In all, 831 women, aged 14–37 of menstrual endometrium and/or at least two plasma cells per years with clinically suspected PID, were recruited from emer- ×120 in the endometrial stroma. For this current substudy, gency departments, OB/GYN clinics, STI clinics and private archived endometrial biopsy and cervical swab specimens were practices in 13 sites throughout the Eastern, Southern and thawed, purified using the MasterPure DNA purification kit for Central regions of the USA. Recruitment
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